The exonuclease ISG20 mainly localizes in the nucleolus and the Cajal (coiled) bodies and is associated with nuclear SMN protein-containing complexes

Journal of Cellular Biochemistry

Volumn 98, Issue 5, 2006, Pages 1320-1333

  Espert, Lucile ^a   Eldin, Patrick ^a   Gongora, Céline ^a   Bayard, Bernard ^a   Harper, Francis ^b   Chelbi Alix, Mounira K ^b   Bertrand, Edouard ^c   Degols, Geneviève ^a   Mechti, Nadir ^a  

^a ETABLISSEMENT FRANÇAIS DU SANG   (France)

^b INSTITUT ANDRÉ LWOFF   (France)

^c INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

Cajal bodies; Exonuclease; Interferon; ISG20; SMN

Indexed keywords

EXONUCLEASE; RED FLUORESCENT PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; SURVIVAL MOTOR NEURON PROTEIN;

ARTICLE; BIOGENESIS; COILED BODY; COMPLEX FORMATION; ELECTRON MICROSCOPY; GENE INDUCTION; HUMAN; HUMAN CELL; MACROMOLECULE; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS INHIBITION; RNA PROCESSING;

CELL NUCLEOLUS; COILED BODIES; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EXONUCLEASES; HELA CELLS; HUMANS; INTERFERONS; MICROSCOPY, IMMUNOELECTRON; NERVE TISSUE PROTEINS; PROTEIN BINDING; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS;

EID: 33746458898     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.20869     Document Type: Article

References (88)

1. Andersen JS, Lyon CE, Fox AH, Leung AK, Lam YW, Steen H, Mann M, Lamond AI. 2002. Directed proteomic analysis of the human nucleolus. Curr Biol 12:1-11.
2. Andrade LE, Chan EK, Raska I, Peebles CL, Roos G, Tan EM. 1991. Human autoantibody to a novel protein of the nuclear coiled body: Immunological characterization and cDNA cloning of p80-coilin. J Exp Med 173:1407-1419.
3. Beelman CA, Parker R. 1995. Degradation of mRNA in eukaryotes. Cell 81:179-183.
4. Bellini M. 2000. Coilin, more than a molecular marker of the cajal (coiled) body. Bioessays 22:861-867.
5. Borden KL. 2002. Pondering the promyelocytic leukemia protein (PML) puzzle: Possible functions for PML nuclear bodies. Mol Cell Biol 22:5259-5269.
6. Boulon S, Basyuk E, Blanchard JM, Bertrand E, Verheggen C. 2002. Intra-nuclear RNA trafficking: Insights from live cell imaging. Biochimie 84:805-813.
7. Cajal SR. 1903. Un sencillo método de coloracion selectiva del reticulo protoplasmico y sus efectos in los diversos organos nerviosos de vertebrados e invertebrados. Tra Lab Invest Biol 2:129-221.
8. Carmo-Fonseca M. 2002a. The contribution of nuclear compartmentalization to gene regulation. Cell 108: 513-521.
9. Carmo-Fonseca M. 2002b. New clues to the function of the Cajal body. EMBO Rep 3:726-727.
10. Carmo-Fonseca M. 2002c. Understanding nuclear order. Trends Biochem Sci 27:332-334.
11. Carvalho T, Almeida F, Calapez A, Lafarga M, Berciano MT, Carmo-Fonseca M. 1999. The spinal muscular atrophy disease gene product, SMN: A link between snRNP biogenesis and the Cajal (coiled) body. J Cell Biol 147:715-728.
12. Chen M, von Mikecz A. 2000. Specific inhibition of rRNA transcription and dynamic relocation of fibrillarin induced by mercury. Exp Cell Res 259:225-238.
13. Cockell MM, Gasser SM. 1999. The nucleolus: Nucleolar space for RENT. Curr Biol 9:R575-R576.
14. Darzacq X, Jady BE, Verheggen C, Kiss AM, Bertrand E, Kiss T. 2002. Cajal body-specific small nuclear RNAs: A novel class of 2′-O-methylation and pseudouridylation guide RNAs. Embo J 21:2746-2756.
15. Deutscher MP, Li Z. 2001. Exoribonucleases and their multiple roles in RNA metabolism. Prog Nucleic Acid Res Mol Biol 66:67-105.
16. Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA, Wehner KA, Wormsley S, Settlage RE, Shabanowitz J, Osheim Y, Beyer AL, Hunt DF, Baserga SJ. 2002. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417:967-970.
17. Dundr M, Misteli T. 2001. Functional architecture in the cell nucleus. Biochem J 356:297-310.
18. Dundr M, Misteli T. 2002. Nucleolomics: An inventory of the nucleolus. Mol Cell 9:5-7.
19. Eppens NA, Faber AW, Rondaij M, Jahangir RS, van Hemert S, Vos JC, Venema J, Raue HA. 2002. Deletions in the S1 domain of Rrp5p cause processing at a novel site in ITS1 of yeast pre-rRNA that depends on Rex4p. Nucleic Acids Res 30:4222-4231.
20. Espert L, Degols G, Gongora C, Blondel D, Williams BR, Silverman RH, Mechti N. 2003. ISG20, a new interferon-induced RNase specific for single-stranded RNA, defines an alternative antiviral pathway against RNA genomic viruses. J Biol Chem 278:16151-16158.
21. Fischer U, Liu Q, Dreyfuss G. 1997. The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis. Cell 90:1023-1029.
22. Gale M, Jr., Katze MG. 1998. Molecular mechanisms of Interferon resistance mediated by viral- directed inhibition of PKR, the interferon-induced protein kinase. Pharmacol Ther 78:29-46.
23. Gall JG. 2000. Cajal bodies: The first 100 years. Annu Rev Cell Dev Biol 16:273-300.
24. Gall JG. 2001. A role for Cajal bodies in assembly of the nuclear transcription machinery. FEBS Lett 498:164-167.
25. Gall JG, Bellini M, Wu Z, Murphy C. 1999. Assembly of the nuclear transcription and processing machinery: Cajal bodies (coiled bodies) andtranscriptosomes. Mol Biol Cell 10:4385-4402.
26. Gerbi SA, Borovjagin A. 1997. U3 snoRNA may recycle through different compartments of the nucleolus. Chromosoma 105:401-406.
27. Gongora C, David G, Pintard L, Tissot C, Hua TD, Dejean A, Mechti N. 1997. Molecular cloning of a new interferon-induced PML nuclear body-associated protein. J Biol Chem 272:19457-19463.
28. Gongora C, Degols G, Espert L, Hua TD, Mechti N. 2000. A unique ISRE, in the TATA-less human Isg20 promoter, confers IRF-1-mediated responsiveness to both interferon type I and type II. Nucleic Acids Res 28:2333-2341.
29. Hebert MD, Szymczyk PW, Shpargel KB, Matera AG. 2001. Coilin forms the bridge between Cajal bodies and SMN, the spinal muscular atrophy protein. Genes Dev 15:2720-2729.
30. Hebert MD, Shpargel KB, Ospina JK, Tucker KE, Matera AG. 2002. Coilin methylation regulates nuclear body formation. Dev Cell 3:329-337.
31. Herrera-Esparza R, Kruse L, Von Essen M, Campos L, Barbosa O, Bollain JJ, Badillo I, Avalos-Diaz E. 2002. U3 snoRNP associates with fibrillarin a component of the scleroderma clumpy nucleolar domain. Arch Dermatol Res 294:310-317.
32. Hiscox JA. 2002. The nucleolus-a gateway to viral infection? Arch Virol 147:1077-1089.
33. Jady BE, Darzacq X, Tucker KE, Matera AG, Bertrand E, Kiss T. 2003. Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm. Embo J 22:1878-1888.
34. Jarrous N, Wolenski JS, Wesolowski D, Lee C, Altman S. 1999. Localization in the nucleolus and coiled bodies of protein subunits of the ribonucleoprotein ribonuclease P. J Cell Biol 146:559-572.
35. Jones KW, Gorzynski K, Hales CM, Fischer U, Badbanchi F, Terns RM, Terns MP. 2001. Direct interaction of the spinal muscular atrophy disease protein SMN with the small nucleolar RNA-associated protein fibrillarin. J Biol Chem 276:38645-38651.
36. Kadowaki T, Schneiter R, Hitomi M, Tartakoff AM. 1995. Mutations in nucleolar proteins lead to nucleolar accumulation of polyA+ RNA in Saccharomyces cerevisiae. Mol Biol Cell 6:1103-1110.
37. Kressler D, Linder P, de La Cruz J. 1999. Protein transacting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol 19:7897-7912.
38. Lam YW, Lyon CE, Lamond AI. 2002. Large-scale isolation of Cajal bodies from HeLa cells. Mol Biol Cell 13:2461-2473.
39. Lamond AI, Earnshaw WC. 1998. Structure and function in the nucleus. Science 280:547-553.
40. Lefebvre S, Burlet P, Viollet L, Bertrandy S, Huber C, Belser C, Munnich A. 2002. A novel association of the SMN protein with two major non-ribosomal nucleolar proteins and its implication in spinal muscular atrophy. Hum Mol Genet 11:1017-1027.
41. Lengyel P. 1993. Tumor-suppressor genes: News about the Interferon connection. Proceedings of the National Academy of Sciences of the United States of America 90:5893-5895.
42. Liu Q, Dreyfuss G. 1996. A novel nuclear structure containing the survival of motor neurons protein. Embo J 15:3555-3565.
43. Liu Q, Fischer U, Wang F, Dreyfuss G. 1997. The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell 90:1013-1021.
44. Liu CJ, Wang H, Lengyel P. 1999. The interferon-inducible nucleolar p204 protein binds the ribosomal RNA-specific UBF1 transcription factor and inhibits ribosomal RNA transcription. Embo J 18:2845-2854.
45. Lyon CE, Bohmann K, Sleeman J, Lamond AI. 1997. Inhibition of protein dephosphorylation results in the accumulation of splicing snRNPs and coiled bodies within the nucleolus. Exp Cell Res 230:84-93.
46. Massenet S, Pellizzoni L, Paushkin S, Mattaj IW, Dreyfuss G. 2002. The SMN complex is associated with snRNPs throughout their cytoplasmic assembly pathway. Mol Cell Biol 22:6533-6541.
47. Matera AG. 1999. Nuclear bodies: Multifaceted subdomains of the interchromatin space. Trends Cell Biol 9:302-309.
48. Matera AG, Frey MR. 1998. Coiled bodies and gems: Janus or gemini? Am J Hum Genet 63:317-321.
49. Matthews DA. 2001. Adenovirus protein V induces redistribution of nucleolin and B23 from nucleolus to cytoplasm. J Virol 75:1031-1038.
50. Maul GG, Negorev D, Bell P, Ishov AM. 2000. Review: Properties and assembly mechanisms of ND10, PML bodies, or PODs. J Struct Biol 129:278-287.
51. Meister G, Buhler D, Laggerbauer B, Zobawa M, Lottspeich F, Fischer U. 2000. Characterization of a nuclear 20S complex containing the survival of motor neurons (SMN) protein and a specific subset of spliceosomal Sm proteins. Hum Mol Genet 9:1977-1986.
52. Meurs E, Chong K, Galabru J, Thomas NS, Kerr IM, Williams BR, Hovanessian AG. 1990. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62:379-390.
53. Moser MJ, Holley WR, Chatterjee A, Mian IS. 1997. The proofreading domain of Escherichia coli DNA polymerase I and other DNA and/or RNA exonuclease domains. Nucleic Acids Res 25:5110-5118.
54. Narayanan A, Speckmann W, Terns R, Terns MP. 1999. Role of the box C/D motif in localization of small nucleolar RNAs to coiled bodies and nucleoli. Mol Biol Cell 10:2131-2147.
55. Narayanan U, Ospina JK, Frey MR, Hebert MD, Matera AG. 2002. SMN, the spinal muscular atrophy protein, forms a pre-import snRNP complex with snurportin1 and importin beta. Hum Mol Genet 11:1785-1795.
56. Negorev D, Maul GG. 2001. Cellular proteins localized at and interacting within ND10/PML nuclear bodies/PODs suggest functions of a nuclear depot. Oncogene 20:7234-7242.
57. Nguyen LH, Espert L, Mechti N, Wilson DM III. 2001. The human interferon- and estrogen-regulated ISG20/ HEM45 gene product degrades single-stranded RNA and DNA in vitro. Biochemistry 40:7174-7179.
58. Ogg SC, Lamond AI. 2002. Cajal bodies and coilin-moving towards function. J Cell Biol 159:17-21.
59. Olson MO, Dundr M, Szebeni A. 2000. The nucleolus: An old factory with unexpected capabilities. Trends Cell Biol 10:189-196.
60. Pederson T. 1998. The plurifunctional nucleolus. Nucleic Acids Res 26:3871-3876.
61. Pellizzoni L, Baccon J, Charroux B, Dreyfuss G. 2001. The survival of motor neurons (SMN) protein interacts with the snoRNP proteins fibrillarin and GAR1. Curr Biol 11:1079-1088.
62. Platani M, Goldberg I, Swedlow JR, Lamond AI. 2000. In vivo analysis of Cajal body movement, separation, and joining in live human cells. J Cell Biol 151:1561-1574.
63. Player MR, Torrence PF. 1998. The 2-5A system: Modulation of viral and cellular processes through acceleration of RNA degradation. Pharmacol Ther 78:55-113.
64. Puvion-Dutilleul F, Mazan S, Nicoloso M, Pichard E, Bachellerie JP, Puvion E. 1992. Alterations of nucleolar ultrastructure and ribosome biogenesis by actinomycin D. Implications for U3 snRNP function. Eur J Cell Biol 58:149-162.
65. Raue HA, Planta RJ. 1991. Ribosome biogenesis in yeast. Prog Nucleic Acid Res Mol Biol 41:89-129.
66. Samarsky DA, Fournier MJ, Singer RH, Bertrand E. 1998. The snoRNA box C/D motif directs nucleolar targeting and also couples snoRNA synthesis and localization. Embo J 17:3747-3757.
67. Scheer U, Hock R. 1999. Structure and function of the nucleolus. Curr Opin Cell Biol 11:385-390.
68. Schneiter R, Kadowaki T, Tartakoff AM. 1995. mRNA transport in yeast: Time to reinvestigate the functions of the nucleolus. Mol Biol Cell 6:357-370.
69. Schofer C, Weipoltshammer K, Almeder M, Muller M, Wachtler F. 1996. Redistribution of ribosomal DNA after blocking of transcription induced by actinomycin D. Chromosome Res 4:384-391.
70. Shaw PJ, Jordan EG. 1995. The nucleolus. Annu Rev Cell Dev Biol 11:93-121.
71. Shpargel KB, Ospina JK, Tucker KE, Matera AG, Hebert MD. 2003. Control of Cajal body number is mediated by the coilin C-terminus. J Cell Sci 116:303-312.
72. Sleeman J, Lyon CE, Platani M, Kreivi JP, Lamond AI. 1998. Dynamic interactions between splicing snRNPs, coiled bodies and nucleoli revealed using snRNP protein fusions to the green fluorescent protein. Exp Cell Res 243:290-304.
73. Sleeman JE, Ajuh P, Lamond AI. 2001. snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J Cell Sci 114:4407-4419.
74. Sleeman JE, Trinkle-Mulcahy L, Prescott AR, Ogg SC, Lamond AI. 2003. Cajal body proteins SMN and Coilin show differential dynamic behaviour in vivo. J Cell Sci 116:2039-2050.
75. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. 1998. How cells respond to interferons. Annu Rev Biochem 67:227-264.
76. Terns MP, Terns RM. 2001. Macromolecular complexes: SMN-the master assembler. Curr Biol 11:862-864.
77. Tollervey D, Kiss T. 1997. Function and synthesis of small nucleolar RNAs. Curr Opin Cell Biol 9:337-342.
78. Tourriere H, Chebli K, Tazi J. 2002. mRNA degradation machines in eukaryotic cells. Biochimie 84:821-837.
79. Tsukamoto T, Hashiguchi N, Janicki SM, Tumbar T, Belmont AS, Spector DL. 2000. Visualization of gene activity in living cells. Nat Cell Biol 2:871-878.
80. Tucker KE, Berciano MT, Jacobs EY, LePage DF, Shpargel KB, Rossire JJ, Chan EK, Lafarga M, Conlon RA, Matera AG. 2001. Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J Cell Biol 154:293-307.
81. van Hoof A, Lennertz P, Parker R. 2000. Three conserved members of the RNase D family have unique and overlapping functions in the processing of 5S, 5.8S, U4, U5, RNase MRP and RNase P RNAs in yeast. Embo J 19:1357-1365.
82. Venema J, Tollervey D. 1996. RRP5 is required for formation of both 18S and 5.8S rRNA in yeast. Embo J 15:5701-5714.
83. Verheggen C, Lafontaine DL, Samarsky D, Mouaikel J, Blanchard JM, Bordonne R, Bertrand E. 2002. Mammalian and yeast U3 snoRNPs are matured in specific and related nuclear compartments. Embo J 21:2736-2745.
84. Wehner KA, Ayala L, Kim Y, Young PJ, Hosler BA, Lorson CL, Baserga SJ, Francis JW. 2002. Survival motor neuron protein in the nucleolus of mammalian neurons. Brain Res 945:160-173.
85. Williams BR. 2001. Signal integration via PKR. Sci STKE 2001:RE2.
86. Young PJ, Le TT, Dunckley M, Nguyen TM, Burghes AH, Morris GE. 2001. Nuclear gems and Cajal (coiled) bodies in fetal tissues: Nucleolar distribution of the spinal muscular atrophy protein, SMN. Exp Cell Res 265:252-261.
87. Zhou A, Hassel BA, Silverman RH. 1993. Expression cloning of 2-5A-dependent RNAase: A uniquely regulated mediator of interferon action. Cell 72:753-765.
88. Zuo Y, Deutscher MP. 2001. Exoribonuclease superfamilies: Structural analysis and phylogenetic distribution. Nucleic Acids Res 29:1017-1026.